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Mechanisms Linking Cytosine Methylation to Histone Modification in Arabidopsis thaliana

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Non Coding RNAs in Plants

Part of the book series: RNA Technologies ((RNATECHN))

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Abstract

Histone modification is the key event in epigenetic regulation of gene expression in most eukaryotes. Plants, fungi, and vertebrates have machineries for DNA methylation as an additional layer of epigenetic modification, and the presence of CHH and CHG (H  =  A, T, or C) methylation sites are characteristics of plants. In Arabidopsis thaliana, both CHH and CHG methylation sites are enriched with sequences related to transposons in heterochromatin regions, and the RNA-directed DNA methylation pathway plays a major role in asymmetric cytosine (CHH) methylation. Heterochromatin regions are also rich in dimethylated histone H3 lysine 9 (H3K9me2) – a histone mark of inert chromatin. Although enzymes transferring methyl groups to DNA or H3K9 have been identified, mechanisms ­linking these two methylation steps specifically to inert chromatin are obscure. In this chapter, we review characteristics of the machineries governing DNA methylation and histone modification in A. thaliana and discuss the possible interplay between these two epigenetic marks in relation to suppression of non coding RNA production.

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Abbreviations

CMM2:

Conserved MOM1 Motif 2

CMT3:

CHROMOMETHYLASE3

DME:

DEMETER

Dnmt1:

DNA METHYLTRANSFERASE1

DRM2:

DOMAINS REARRANGED METHYLTRANSFERASE2

H3K9me2:

Di-methylated histone H3 lysine 9

HDAC:

Histone deacetylase

IBM1:

INCREASE IN BONSAI METHYLATION1

KYP:

KRYPTONITE

MBD:

Methyl-CpG-binding domain

MBT:

Malignant brain tumor

MET1:

METHYLTRANSFERASE1

MOM1:

MORPHEUS’ MOLECULE1

ORTH:

ORTHRUS

PcG:

Polycomb group

PHD:

Plant homeo domain

Pol:

RNA polymerase

PRC2:

Polycomb repressive complex2

RdDM:

RNA-directed DNA methylation

siRNA:

Small interfering RNA

SRA:

SET and RING associated

SUVH:

SU(VAR)3-9 HOMOLOGUE

TGS:

Transcriptional gene silencing

trxG:

Trithorax group

UHRF1:

UBIQUITIN-LIKE, CONTAINING PHD AND RING FINGER DOMAINS 1

VIM:

VARIANT IN METHYLATION

References

  • Ahmad A, Zhang Y, Cao XF (2010) Decoding the epigenetic language of plant development. Mol Plant 3:719–728

    Article  PubMed  CAS  Google Scholar 

  • Amedeo P, Habu Y, Afsar K et al (2000) Disruption of the plant gene MOM releases transcriptional silencing of methylated genes. Nature 405:203–206

    Article  PubMed  CAS  Google Scholar 

  • Arita K, Ariyoshi M, Tochio H et al (2008) Recognition of hemi-methylated DNA by the SRA protein UHRF1 by a base-flipping mechanism. Nature 455:818–821

    Article  PubMed  CAS  Google Scholar 

  • Aufsatz W, Mette MF, van der Winden J et al (2002) HDA6, a putative histone deacetylase needed to enhance DNA methylation induced by double-stranded RNA. EMBO J 21:6832–6841

    Article  PubMed  CAS  Google Scholar 

  • Avramova Z (2009) Evolution and pleiotropy of TRITHORAX function in Arabidopsis. Int J Dev Biol 53:371–381

    Article  PubMed  CAS  Google Scholar 

  • Avvakumov GV, Walker JR, Xue S et al (2008) Structural basis for recognition of hemi-methylated DNA by the SRA domain of human UHRF1. Nature 455:822–825

    Article  PubMed  CAS  Google Scholar 

  • Bartee L, Malagnac F, Bender J (2001) Arabidopsis cmt3 chromomethylase mutations block non-CG methylation and silencing of an endogenous gene. Genes Dev 15:1753–1758

    Article  PubMed  CAS  Google Scholar 

  • Belostotsky DA, Sieburth LE (2009) Kill the messenger: mRNA decay and plant development. Curr Opin Plant Biol 12:96–102

    Article  PubMed  CAS  Google Scholar 

  • Bogdanović O, Veenstra GJ (2009) DNA methylation and methyl-CpG binding proteins: developmental requirements and function. Chromosoma 118:549–565

    Article  PubMed  CAS  Google Scholar 

  • Bostick M, Kim JK, Estève PO et al (2007) UHRF1 plays a role in maintaining DNA methylation in mammalian cells. Science 317:1760–1764

    Article  PubMed  CAS  Google Scholar 

  • Bowen NJ, Fujita N, Kajita M et al (2004) Mi-2/NuRD: multiple complexes for many purposes. Biochim Biophys Acta 1677:52–57

    Article  PubMed  CAS  Google Scholar 

  • Čaikovski M, Yokthongwattana C, Habu Y et al (2008) Divergent evolution of CHD3 proteins resulted in MOM1 refining epigenetic control in vascular plants. PLoS Genet 4:e1000165

    Article  PubMed  Google Scholar 

  • Cedar H, Bergman Y (2009) Linking DNA methylation and histone modification: patterns and paradigms. Nat Rev Genet 10:295–304

    Article  PubMed  CAS  Google Scholar 

  • Chen X (2010) Small RNAs – secrets and surprises of the genome. Plant J 61:941–958

    Article  PubMed  CAS  Google Scholar 

  • Cheng X, Blumenthal RM (2010) Coordinated chromatin control: structural and functional linkage of DNA and histone methylation. Biochemistry 49:2999–3008

    Article  PubMed  CAS  Google Scholar 

  • Cokus SJ, Feng S, Zhang X et al (2008) Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452:215–219

    Article  PubMed  CAS  Google Scholar 

  • Earley KW, Pontvianne F, Wierzbicki AT et al (2006) Mechanisms of HDA6-mediated rRNA gene silencing: Suppression of intergenic Pol II transcription and differential effects on maintenance versus siRNA-directed cytosine methylation. Genes Dev 24:1119–1132

    Article  Google Scholar 

  • Ebbs ML, Bender J (2006) Locus-specific control of DNA methylation by the Arabidopsis SUVH5 histone methyltransferase. Plant Cell 18:1166–1176

    Article  PubMed  CAS  Google Scholar 

  • Finnegan EJ, Dennis ES (1993) Isolation and identification by sequence homology of a putative cytosine methyltransferase from Arabidopsis thaliana. Nucleic Acids Res 21:2383–2388

    Article  PubMed  CAS  Google Scholar 

  • Garneau NL, Wilusz J, Wilusz CJ (2007) The highways and byways of mRNA decay. Nat Rev Mol Cell Biol 8:113–126

    Article  PubMed  CAS  Google Scholar 

  • Gendrel AV, Lippman Z, Yordan C et al (2002) Dependence of heterochromatic histone H3 methylation patterns on the Arabidopsis gene DDM1. Science 297:1871–1873

    Article  PubMed  CAS  Google Scholar 

  • Grafi G, Zemach A, Pitto L (2007) Methyl-CpG-binding domain (MBD) proteins in plants. Biochim Biophys Acta 1769:287–294

    Article  PubMed  CAS  Google Scholar 

  • Habu Y, Mathieu O, Tariq M et al (2006) Epigenetic regulation of transcription in intermediate heterochromatin. EMBO Rep 7:1279–1284

    Article  PubMed  CAS  Google Scholar 

  • Hashimoto H, Horton JR, Zhang X et al (2008) The SRA domain of UHRF1 flips 5-methylcytosine out of the DNA helix. Nature 455:826–829

    Article  PubMed  CAS  Google Scholar 

  • Ho KL, McNae IW, Schmiedeberg L et al (2008) MeCP2 binding to DNA depends upon hydration at methyl-CpG. Mol Cell 29:525–531

    Article  PubMed  CAS  Google Scholar 

  • Ikeda Y, Kinoshita T (2009) DNA demethylation: a lesson from the garden. Chromosoma 118:37–41

    Article  PubMed  CAS  Google Scholar 

  • Jackson JP, Lindroth AM, Cao X et al (2002) Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416:556–560

    Article  PubMed  CAS  Google Scholar 

  • Jacob Y, Feng S, LeBlanc CA et al (2009) ATXR5 and ATXR6 are H3K27 monomethyltransferases required for chromatin structure and gene silencing. Nat Struct Mol Biol 16:763–768

    Article  PubMed  CAS  Google Scholar 

  • Johnson LM, Law JA, Khattar A et al (2008) SRA-domain proteins required for DRM2-mediated de novo DNA methylation. PLoS Genet 4:e1000280

    Article  PubMed  Google Scholar 

  • Kankel MW, Ramsey DE, Stokes TL et al (2003) Arabidopsis MET1 cytosine methyltransferase mutants. Genetics 163:1109–1122

    PubMed  CAS  Google Scholar 

  • Kraft E, Bostick M, Jacobsen SE et al (2008) ORTH/VIM proteins that regulate DNA methylation are functional ubiquitin E3 ligases. Plant J 56:704–715

    Article  PubMed  CAS  Google Scholar 

  • Law JA, Jacobsen SE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11:204–220

    Article  PubMed  CAS  Google Scholar 

  • Lawrence RJ, Earley K, Pontes O et al (2004) A concerted DNA methylation/histone methylation switch regulates rRNA gene dosage control and nucleolar dominance. Mol Cell 13:599–609

    Article  PubMed  CAS  Google Scholar 

  • Lindroth AM, Cao X, Jackson JP et al (2001) Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science 292:2077–2080

    Article  PubMed  CAS  Google Scholar 

  • Lindroth AM, Shultis D, Jasencakova Z et al (2004) Dual histone H3 methylation marks at lysines 9 and 27 required for interaction with CHROMOMETHYLASE3. EMBO J 23:4286–4296

    Article  PubMed  CAS  Google Scholar 

  • Lippman Z, May B, Yordan C et al (2003) Distinct mechanisms determine transposon inheritance and methylation via small interfering RNA and histone modification. PLoS Biol 1:E67

    Article  PubMed  Google Scholar 

  • Lister R, O’Malley RC, Tonti-Filippini J et al (2008) Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell 133:523–536

    Article  PubMed  CAS  Google Scholar 

  • Loidl P (2004) A plant dialect of the histone language. Trends Plant Sci 9:84–90

    Article  PubMed  CAS  Google Scholar 

  • Lu C, Tej SS, Luo S et al (2005) Elucidation of the small RNA component of the transcriptome. Science 309:1567–1569

    Article  PubMed  CAS  Google Scholar 

  • Malagnac F, Bartee L, Bender J (2002) An Arabidopsis SET domain protein required for maintenance but not establishment of DNA methylation. EMBO J 21:6842–6852

    Article  PubMed  CAS  Google Scholar 

  • Marfella CG, Imbalzano AN (2007) The Chd family of chromatin remodelers. Mutat Res 618:30–40

    Article  PubMed  CAS  Google Scholar 

  • Matzke M, Kanno T, Daxinger L et al (2009) RNA-mediated chromatin-based silencing in plants. Curr Opin Cell Biol 21:367–376

    Article  PubMed  CAS  Google Scholar 

  • Miura A, Nakamura M, Inagaki S et al (2009) An Arabidopsis jmjC domain protein protects transcribed genes from DNA methylation at CHG sites. EMBO J 28:1078–1086

    Article  PubMed  CAS  Google Scholar 

  • Morinière J, Rousseaux S, Steuerwald U et al (2009) Cooperative binding of two acetylation marks on a histone tail by a single bromodomain. Nature 461:664–668

    Article  PubMed  CAS  Google Scholar 

  • Naumann K, Fischer A, Hofmann I et al (2005) Pivotal role of AtSUVH2 in heterochromatic ­histone methylation and gene silencing in Arabidopsis. EMBO J 24:1418–1429

    Article  PubMed  CAS  Google Scholar 

  • Numa H, Kim JM, Matsui A et al (2010) Transduction of RNA-directed DNA methylation signals to repressive histone marks in Arabidopsis thaliana. EMBO J 29:352–362

    Article  PubMed  CAS  Google Scholar 

  • Ohki I, Shimotake N, Fujita N et al (2001) Solution structure of the methyl-CpG binding domain of human MBD1 in complex with methylated DNA. Cell 105:487–497

    Article  PubMed  CAS  Google Scholar 

  • Pien S, Grossniklaus U (2007) Polycomb group and trithorax group proteins in Arabidopsis. Biochim Biophys Acta 1769:375–382

    Article  PubMed  CAS  Google Scholar 

  • Qian C, Zhou MM (2006) Set domain protein lysine methyltransferases: structure, specificity and catalysis. Cell Mol Life Sci 63:2755–2763

    Article  PubMed  CAS  Google Scholar 

  • Richards EJ, Elgin SC (2002) Epigenetic codes for heterochromatin formation and silencing: rounding up the usual suspects. Cell 108:489–500

    Article  PubMed  CAS  Google Scholar 

  • Saze H, Mittelsten Scheid O, Paszkowski J (2003) Maintenance of CpG methylation is essential for epigenetic inheritance during plant gametogenesis. Nat Genet 34:65–69

    Article  PubMed  CAS  Google Scholar 

  • Saze H, Shiraishi A, Miura A et al (2008) Control of genic DNA methylation by a jmjC domain-containing protein in Arabidopsis thaliana. Science 319:462–465

    Article  PubMed  CAS  Google Scholar 

  • Schoft VK, Chumak N, Mosiolek M et al (2009) Induction of RNA-directed DNA methylation upon decondensation of constitutive heterochromatin. EMBO Rep 10:1015–1021

    Article  PubMed  CAS  Google Scholar 

  • Schwartz S, Ast G (2010) Chromatin density and splicing destiny: on the cross-talk between ­chromatin structure and splicing. EMBO J 29:1629–1636

    Article  PubMed  CAS  Google Scholar 

  • Sharif J, Muto M, Takebayashi S et al (2007) The SRA protein Np95 mediates epigenetic inheritance by recruiting Dnmt1 to methylated DNA. Nature 450:908–912

    Article  PubMed  CAS  Google Scholar 

  • Soppe WJ, Jasencakova Z, Houben A et al (2002) DNA methylation controls histone H3 lysine 9 methylation and heterochromatin assembly in Arabidopsis. EMBO J 21:6549–6559

    Article  PubMed  CAS  Google Scholar 

  • Steimer A, Amedeo P, Afsar K et al (2000) Endogenous targets of transcriptional gene silencing in Arabidopsis. Plant Cell 12:1165–1178

    PubMed  CAS  Google Scholar 

  • Tariq M, Habu Y, Paszkowski J (2002) Depletion of MOM1 in non-dividing cells of Arabidopsis plants releases transcriptional gene silencing. EMBO Rep 3:951–955

    Article  PubMed  CAS  Google Scholar 

  • Tariq M, Saze H, Probst AV et al (2003) Erasure of CpG methylation in Arabidopsis alters patterns of histone H3 methylation in heterochromatin. Proc Natl Acad Sci USA 100:8823–8827

    Article  PubMed  CAS  Google Scholar 

  • Taverna SD, Li H, Ruthenburg AJ et al (2007) How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers. Nat Struct Mol Biol 14:1025–1040

    Article  PubMed  CAS  Google Scholar 

  • Vrbsky J, Akimcheva S, Watson JM et al (2010) siRNA-mediated methylation of Arabidopsis telomeres. PLoS Genet 6:e1000986

    Article  PubMed  Google Scholar 

  • Wang Z, Song J, Milne TA et al (2010) Pro isomerization in MLL1 PHD3-bromo cassette connects H3K4me readout to CyP33 and HDAC-mediated repression. Cell 141:1183–1194

    Article  PubMed  CAS  Google Scholar 

  • Wierzbicki AT, Haag JR, Pikaard CS (2008) Noncoding transcription by RNA polymerase Pol IVb/Pol V mediates transcriptional silencing of overlapping and adjacent genes. Cell 135:635–648

    Article  PubMed  CAS  Google Scholar 

  • Woo HR, Pontes O, Pikaard CS et al (2007) VIM1, a methylcytosine-binding protein required for centromeric heterochromatinization. Genes Dev 21:267–277

    Article  PubMed  CAS  Google Scholar 

  • Yelina NE, Smith LM, Jones AM et al (2010) Putative Arabidopsis THO/TREX mRNA export complex is involved in transgene and endogenous siRNA biosynthesis. Proc Natl Acad Sci USA 107:13948–13953

    Article  PubMed  CAS  Google Scholar 

  • Yokthongwattana C, Bucher E, Čaikovski M et al (2010) MOM1 and Pol-IV/V interactions regulate the intensity and specificity of transcriptional gene silencing. EMBO J 29:340–351

    Article  PubMed  CAS  Google Scholar 

  • Zeng L, Zhang Q, Li S et al (2010) Mechanism and regulation of acetylated histone binding by the tandem PHD finger of DPF3b. Nature 466:258–262

    Article  PubMed  CAS  Google Scholar 

  • Zhang X, Yazaki J, Sundaresan A et al (2006) Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126:1189–1201

    Article  PubMed  CAS  Google Scholar 

  • Zheng B, Wang Z, Li S et al (2009) Intergenic transcription by RNA polymerase II coordinates Pol IV and Pol V in siRNA-directed transcriptional gene silencing in Arabidopsis. Genes Dev 23:2850–2860

    Article  PubMed  CAS  Google Scholar 

  • Zilberman D, Gehring M, Tran RK et al (2007) Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat Genet 39:61–69

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Division of Plant Sciences, National Institute of Agrobiological Sciences, Tsukuba, 305-8602, Japan

    Manabu Yoshikawa & Yoshiki Habu

  2. Laboratory of Biomolecular Function Chemistry, Department of Molecular Engineering, Kyoto University, Kyoto, 615-8510, Japan

    Kyohei Arita

  3. School of Natural Sciences, National University of Ireland, Galway, Ireland

    Tatsuo Kanno

Authors
  1. Kyohei Arita
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  2. Tatsuo Kanno
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  3. Manabu Yoshikawa
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  4. Yoshiki Habu
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Corresponding author

Correspondence to Yoshiki Habu .

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Editors and Affiliations

  1. Institute of Chemistry/Biochemistry, Free University Berlin, Thielallee 63, Berlin, 14195, Berlin, Germany

    Volker A. Erdmann

  2. Inst. Bioorganic Chemistry, PAN Poznan, ul. Z. Noskowskiego 12/14, Poznan, 61-704, Poland

    Jan Barciszewski

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Arita, K., Kanno, T., Yoshikawa, M., Habu, Y. (2011). Mechanisms Linking Cytosine Methylation to Histone Modification in Arabidopsis thaliana . In: Erdmann, V., Barciszewski, J. (eds) Non Coding RNAs in Plants. RNA Technologies. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-19454-2_15

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